Protection and restoration of species in the wild may require conservation breeding programs under genetic management to minimize deleterious effects of genetic changes that occur in captivity, while preserving populations' genetic diversity and evolutionary resilience. Here, through interannual pedigree analyses, we first assessed the efficiency of a 21-year genetic management, including minimization of mean kinship, inbreeding avoidance, and regular addition of founders, of a conservation breeding program targeting on Houbara bustard (Chlamydotis undulata undulata) in Morocco. Secondly, we compared pedigree analyses, the classical way of assessing and managing genetic diversity in captivity, to molecular analyses based on seven microsatellites. Pedigree-based results indicated an efficient maintenance of the genetic diversity (99% of the initial genetic diversity retained) while molecularbased results indicated an increase in allelic richness and an increase in unbiased expected heterozygosity across time. The pedigree-based average inbreeding coefficient F remained low (between 0.0004 and 0.003 in 2017) while the proportion of highly inbred individuals (F > .1) decreased over time and reached 0.2% in 2017. Furthermore, pedigree-based F and molecular-based individual multilocus heterozygosity were weakly negatively correlated, (Pearson's r = −.061 when considering all genotyped individuals), suggesting that they cannot be considered as alternatives, but rather as complementary sources of information. These findings suggest that a strict genetic monitoring and management, based on both pedigree and molecular tools can help mitigate genetic changes and allow to preserve genetic diversity and evolutionary resilience in conservation breeding programs.
Although captive breeding programs are valuable for conservation, they have been shown to be associated with genetic changes, such as adaptation to captivity or inbreeding. In addition, reproductive performance is strongly age-dependent in most animal species. These mechanisms that potentially impact reproduction have often been studied separately, while their interactions have rarely been addressed. In this study, using a large dataset of nine male and female reproductive parameters measured for 12,295 captive houbara bustards (Chlamydotis undulata undulata) over 24 years, we investigated the relative and interactive effects of age, inbreeding and number of generations in captivity on reproduction. We clearly identified (1) senescence patterns in all parameters studied; (2) negative effects of inbreeding on sperm characteristics, display behavior, egg weight, egg volume and hatching probability; and (3) changes in phenotypic values for seven parameters according to number of generations in captivity. However, the effect sizes associated with age were substantially greater than those associated with inbreeding and number of generations in captivity. Beyond the independent effects of these three factors on reproductive parameters, the results highlighted their interactive effects and thus the importance of integrating them in the design of genetic management plans for conservation breeding programs.
Conservation breeding programs pursue the double objective of preserving genetic diversity and producing individuals to support in situ conservation measures. Genetic management and monitoring are commonly based on pedigree analyses and are therefore dependent on the pedigree quality and the underlying assumption that founders of the captive population are neither inbred nor related to each other or to the captive population. Should founders be related, this assumption may lead to an overestimation of genetic diversity and an underestimation of inbreeding in captivity. In this study, we examined the effects of the founder assumption on estimates of genetic diversity by combining three approaches: (1) computer simulations of pedigrees of theoretical captive populations and their associated in situ source populations, (2) analysis of pedigrees of real conservation breeding programs and (3) microsatellite‐based computation of kinship among founders from a captive population of houbara bustard. The theoretical approach revealed that the captive population's average mean kinship Mk increases linearly with founder average Mk. The bias in Mk due to the founder assumption was strongly related to the effective size of the source population and to pedigree quality while remaining critical after 25 generations of captivity. Results based on real populations were consistent with theoretical ones and confirmed the overestimation of genetic diversity in captive populations. Overall, our results indicate that under situations classically encountered in conservation breeding programs (e.g. small and isolated source population, incomplete pedigrees), estimates of genetic diversity are potentially highly overestimated, challenging the genetic management of captive populations of species of conservation concern.
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